How phenotypic matching based on neutral mating cues enables speciation in locally adapted populations

Abstract

Maynard Smith's (American Naturalist, 1966, 100, 637) suggestion that in some cases a prerequisite for speciation is the existence of local ecological adaptations has not received much attention to date. Here, we test the hypothesis using a model like that of Maynard Smith but differing in the way animals disperse between niches. In previous studies, males disperse randomly between niches but females stay put in their natal niche. As a first step toward generalizing the model, we here analyze the case that equal proportions of the two sexes disperse between niches before breeding. Supporting Maynard Smith's (1966) hypothesis, we find that once local adaptations are established, a neutral mating cue at an independent locus can rapidly enable speciation in populations with a suitable mechanism for phenotype matching. We find that stable ecological polymorphisms are relatively insensitive to the strength of selection, but depend crucially on the extent of dispersal between niches, with a threshold of ~5% if population sizes in two niches are equal. At higher levels of dispersal, ecological differentiation is lost. These results contrast with those of earlier studies and shed light on why parapatric speciation is limited by the extent of gene flow. Our testable model provides a candidate explanation for the rapid speciation rates, diversity of appearance and occurrence of "species flocks" observed among some African cichlids and neotropical birds and may also have implications for the occurrence of punctuational change on phylogenies.

Keywords: assortative mating; mate choice; parapatric speciation; phenotype matching; population genetics; sexual imprinting.

Figure 1

Conceptual overview of the model. For clarity, the niches are shown distinct, but in nature may be contiguous or overlap. Population sizes in each niche are constant. m ₁₂ and m ₂₁ specify the proportion of individuals in one niche that disperse to the other each generation after viability selection has occurred. Breeding occurs after dispersal. Number of offspring is determined by the product of the fitnesses of the male and the female partners. Carriers of the Q allele have fitnesses f ₁ and f ₂ in niches 1 and 2, respectively, and the fitness of PP homozygotes is set at 1 throughout

Figure 2

Results of running the model when the proportion of individuals in each niche that disperse to the other each generation is 3% per generation, and α = 1. Only three of the nine genotypes are shown. The P and Q alleles are initially at dynamic equilibrium determined by the balance between local adaptation and dispersal between the two niches as shown in Table 2. The C allele is absent before being introduced into niche 2 at a frequency of 1% CDQQ in generation 1. The fitness of carriers of Q in niche 2, f ₂ equals 1.1; their fitness in niche 1, f ₁ = 1/f ₂. Population sizes are the same in the two niches

Figure 3

Final frequencies of key genotypes plotted against the % individuals moving between niches for three values of f ₂. (a and d) f ₂ = 1.05; (b and e) f ₂ = 1.1; (c and f) f ₂ = 1.2. In all panels, f ₁ = 1/f ₂ and α = 1. The P and Q alleles are initially at dynamic equilibrium, and the C allele is absent before being introduced into: top row: niche 2 at a frequency of 1% CDQQ; bottom row niche 1 at a frequency of 1% CDPP. Dots represent outputs of simulations. Population sizes are the same in the two niches

Figure 4

Final frequencies of key genotypes plotted against the % individuals in niche 2 that disperse to niche 1 for the case that (a) niche 1 is 10 times the size of niche 2; (b) niche 1 is one tenth the size of niche 2. Numbers moving each way are assumed the same within each panel. Symbols and initial values calculated as in Figure 3. f ₂ = 1.2; f ₁ = 1/f ₂ and α = 1. C allele absent before being introduced into niche 2 at a frequency of 1% CDQQ